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Frogs and toads (Anura) Franky Bossuyt and Kim Roelants of molecular phylogenetic studies is now leading to an Biology Department, Unit of Ecology & Systematics, Amphibian increasingly resolved consensus for the anuran tree. In Evolution Lab, Vrije Universiteit Brussel, Pleinlaan 2, 1050 Brussels, this chapter, we review the relationships and divergence Belgium times among 59 anuran families and argue that their *To whom correspondence should be addressed (fbossuyt@vub. evolutionary history is largely congruent with major ac.be) geological and environmental changes in Earth’s history. We mostly implement clade and family names derived Abstract from the taxonomy recently proposed by Frost et al. (3). However, we believe that evolutionary time is an import- Anura (frogs and toads) constitute over 90% of living ant parameter in conveying useful comparative infor- amphibian diversity. Recent timetree constructions have mation in biological classiA cation (4). We therefore treat shown that their diversifi cation was a highly episodic pro- Ascaphidae, Discoglossidae, Nasikabatrachidae, some cess, with establishment of the major clades in three peri- subfamilies in Nobleobatrachia, and all subfamilies of ods: Triassic (251–200 million years ago, Ma), end of Jurassic Microhylidae sensu lato as distinct families. to early Cretaceous (~150–100 Ma), and end of Cretaceous 7 e sequence of early divergences in Anura has been to early Paleogene (~70–50 Ma). The early diversifi cation the subject of major controversy. Most of the debate of anurans predated the initial north–south breakup of focused on the phylogenetic position of archaeobatra- Pangaea, and resulted in distinct assemblages in both hemi- chian families (taxa with primitive or transitional char- spheres. The subsequent radiation of neobatrachian frogs acters, covering ~4% of all extant species) with respect has been largely determined by Gondwanan fragmenta- to neobatrachian families (“advanced” taxa, covering tion and resulted in recurrent patterns of continent-scale endemism. Anura (Fig. 1) (“tail-less amphibians”) represent the lar- gest living order of amphibians, and currently include ~5400 described species (1). Most of them undergo the typical amphibious life history and are dependent on the presence of water for their reproduction and devel- opment. Multiple lineages, however, show an evolution- ary trend toward increased terrestriality in larval or adult frog stages. Despite an evolutionarily conserved body plan, anurans have diversiA ed into a myriad of eco- morphs and have adapted to life in habitats as distinct as rainforest canopies, mangroves, and sand dune burrows. In addition, anurans have attained a subcosmopolitan distribution and are currently only absent in extreme northern latitudes, Antarctica, and most oceanic (non- continental) islands (2). 7 e independent occupation of similar ecological niches by frog taxa in diB erent geo- graphic regions has resulted in extraordinary cases of evolutionary convergence. 7 e consequent high levels of morphological homoplasy have complicated anuran sys- Fig. 1 A tree frog (Rhacophorus lateralis) from India. Credit: tematics for decades. However, a major ongoing upsurge F. Bossuyt. F. Bossuyt and K. Roelants. Frogs and toads (Anura). Pp. 357–364 in e Timetree of Life, S. B. Hedges and S. Kumar, Eds. (Oxford University Press, 2009). HHedges.indbedges.indb 335757 11/28/2009/28/2009 11:28:26:28:26 PPMM 358 THE TIMETREE OF LIFE Microhylidae 43 Dyscophidae 37 Asterophryidae 35 Kalophrynidae 46 Cophylidae 44 32 Melanobatrachidae Gastrophrynidae Microhyloidea 31 Scaphiophrynidae 28 Hoplophrynidae 25 Phrynomeridae 17 Arthroleptidae 42 26 Astylosternidae Hyperoliidae 21 Brevicipitidae 38 Afrobatrachia Hemisotidae Mantellidae 41 Neobatrachia Rhacophoridae 36 16 Dicroglossidae 33 39 Ranidae Nyctibatrachidae 29 Micrixalidae 40 Ranixalidae 34 24 Ceratobatrachidae Natatanura 11 Petropedetidae 23 30 Pyxicephalidae 27 Phrynobatrachidae Ptychadenidae Sooglossidae 22 Nasikabatrachidae Triassic Jurassic Cretaceous Pg Ng Sooglossoidea MESOZOIC CENOZOIC 250 200 150 100 50 0 Million years ago Fig. 2 Continues the remaining 96% of extant species). Morphological (Archaeobatrachia) as the closest relatives of Neo- studies have supported diverse paraphyletic arrange- batrachia (11–13). Recent phylogenetic studies, imple- ments of archaeobatrachian families (5–10). Although menting expanded taxon sampling, nuclear and Neobatrachia have traditionally been considered to con- mitochondria l protein-coding DNA sequences, and mod- stitute a single-nested clade, analyses of combined lar- el-based reconstruction methods, have provided robust val and adult characters have recently questioned their support for a paraphyletic arrangement of four major monophyly (9, 10). archaeobatrachian lineages: (i) Amphicoela: Ascaphidae Early analyses of ribosomal DNA sequences clus- + Leiopelmatidae, (ii) Costata (previously known as tered the archaeobatrachian families in a single clade Discoglossoidea), (iii) Xenoanura (Pipoidea), and (iv) HHedges.indbedges.indb 335858 11/28/2009/28/2009 11:28:30:28:30 PPMM Eukaryota; Metazoa; Vertebrata; Lissamphibia; Anura 359 (continued from previous page) Pelodryadidae 56 Phyllomedusidae 52 Brachycephalidae Craugastoridae 10 55 51 Eleutherodactylidae Strabomantidae 49 Hylidae 54 Ceratophryidae Telmatobiidae 47 Nobleobatrachia Bufonidae 53 Dendrobatidae 9 45 48 Leptodactylidae 50 Centrolenidae Rhinodermatidae 13 Neobatrachia Limnodynastidae 20 Rheobatrachidae 19 4 15 Myobatrachidae Calyptocephalellidae Myobatrachoidea Heleophrynidae Pelobatidae 3 18 14 Megophryidae 8 Pelodytidae Scaphiopodidae Anomocoela 2 Pipidae 7 Rhinophrynidae Alytidae Xenoanura 12 1 6 Discoglossidae Bombinatoridae Costata Ascaphidae 5 Leiopelmatidae Amphicoela Triassic Jurassic Cretaceous Pg Ng MESOZOIC CENOZOIC 250 200 150 100 50 0 Million years ago Fig. 2 A timetree of frogs and toads (Anura). Divergence times are shown in Table 1 Ng (Neogene), Pg (Paleogene), and Tr (Triassic).. Anomocoela (Pelobatoidea) (3, 14–18). Consistent with (14), of an Anomocoela + Neobatrachia clade (16–18), most morphological evidence, they supported the basal and of a Costata + Anomocoela + Neobatrachia clade divergence of Amphicoela, and identiA ed Anomocoela as (3, 15). the closest relative of Neobatrachia. A remaining point 7 e monophyly of Neobatrachia has always received of ambiguity is the phylogenetic position of Xenoanura. strong support from molecular data ( 3, 12–22). Vari- Molecular studies have variously resolved Xenoanura as ous arrangements of the following four well-supported the closest relative of Costata (17, 19), of Neobatrachia lineages have been published: (i) Heleophrynidae, HHedges.indbedges.indb 335959 11/28/2009/28/2009 11:28:31:28:31 PPMM 360 THE TIMETREE OF LIFE Table 1. Divergence times (Ma) and their 95% confi dence/credibility intervals (CI) among anurans. Timetree Estimates Node Time Ref. (15) Ref. (18) Ref. (26) Ref. (30) Ref. (37) (Fig. 2) (Ma) Time CI Time CI Time Time CI Time 1 243 262 304–223 243 264–217 – – – – 2 234 245 288–204 234 258–210 183 – – – 3229––229253–204–––– 4 222 216 260–176 222 247–197 – – – – 5 203 237 281–193 203 227–177 172 – – – 6 203 199 244–155 203 228–180 132 – – – 7193––193218–170–––– 8 167 164 208–121 167 191–146 127 – – – 9 167 162 199–128 167 186–149 125 – – – 10 161 150 186–117 161 180–143 – – – – 11 159 131 167–99 159 178–141 110 – – – 12 152 152 199–105 152 179–129 – – – – 13 146 138 172–108 146 164–129 106 – – – 14 143 142 187–101 143 166–121 112 – – – 15 129 120 154–91 129 147–113 94.4 – – – 16 119 99 132–70 119 131–106 – 133 154–115 – 17 117 – – 117 129–104 – 127 148–110 – 18 115 118 162–77 115 136–93 93.3 – – – 19107––107123–89–––– 20102––102118–85–––– 21 102 – – 102 115–90 – 107 126–89 – 22101––101121–83–––– 23 94.4 – – 82.5 95–71 – 94.4 113–78 – 2489.7–––––89.7108–74– 25 88 – – 75.6 83–70 – 88 102–77 – 26 87.7 – – 87.7 100–75 – 96 117–78 – 2786.3–––––86.3104–71– 2883.9–––––83.997–74– 2982.9–––––82.9100–68– 30 81.1 – – 72.6 85–62 – 81.1 99–66 – 3180.5–––––80.593–72– 3279–––––7991–70– 3378.1–––––78.195–64– 3477.6–––––77.695–63– 35 76.8 – – 73.0 79–68 – 76.8 89–69 – 36 74.4 – – 70.3 81–60 – 74.4 91–61 – 37 73.6 – – 70.2 76–66 – 73.6 85–67 – 38 72.1 – – 72.1 85–59 – 74.6 94–58 – 3971.7–––––71.788–58– 40 71.2 – – – – – 71.2 89–56 – HHedges.indbedges.indb 336060 11/28/2009/28/2009 11:28:31:28:31 PPMM Eukaryota; Metazoa; Vertebrata; Lissamphibia; Anura 361 Table 1. Continued Timetree Estimates Node Time Ref. (15) Ref. (18) Ref. (26) Ref. (30) Ref. (37) (Fig. 2) (Ma) Time CI Time CI Time Time CI Time 41 69.7 – – 62.8 74–53 – 69.7 86–56 – 42 69.1 – – 69.1 81–57 – – – – 43 68.7 – – 67.1 71–66 – 68.7 78–65 – 4466.8–––––66.880–56– 4563––6377–53–––– 4661.8–––––61.876–49– 4761.1––61.176–51–––– 4859.7––59.774–50–––– 4958.4––58.472–49–––– 5057.9––57.972–49–––– 5156.7––56.770–47–––– 5255––5568–46–––– 5354.6––54.668–45–––– 5453.2––53.266–44–––– 5546.5–––––––46.5 56 43.2 – – 43.2 55–36 – – – – Note: Node times in the timetree are based on refs. (18) and (30) for Natatanura and Microhyloidea, because the use of time estimates averaged across all studies would be incompatible with the depicted topology. (ii) Sooglossoidea: Nasikabatrachidae + Sooglossidae, Calyptocephalella (= Caudiverbera) and Telmatobufo (iii) Nobleobatrachia (the “Hyloidea” of 14, 15, 21) + Myo- (both now Calyptocephalellidae) of Chile as the closest batrachoidea + Calyptocephalellidae, and (iv) Ranoides: relatives of the Australo-Papuan Myobatrachoidea (3, 15, Afrobatrachia + Microhyloidea + Natatanura. Most 18, 24). 7 e same analyses recovered this previously studies of the past few years have converged on a basal unrecognized clade (Australobatrachia) as the clos- split between the South African endemic Heleophry- est relatives of Nobleobatrachia. Several controversies nidae and the remaining neobatrachians (3, 14–18). An however remain in nobleobatrachian phylogeny: A rst, important addition to the amphibian tree resulted from Leptodactylidae as deA ned here was not found mono- the discovery of a new frog lineage (Nasikabatrachidae) phyletic in a recent molecular study (25), although this in the Western Ghats of India (21).